Subterranean Fishes of the World

6789

2024

Proceedings of the National Academy of Sciences

1-10

121 49 e2415854121

Copyright © 2024 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

The ability to follow the evolutionary trajectories of specific neuronal cell types has led to major insights into the evolution of the vertebrate brain. Here, we study how cave life in the Mexican tetra (Astyanax mexicanus) has affected an identified giant multisensory neuron, the Mauthner neuron (MN). Because this neuron is crucial in driving rapid escapes, the absence of predation risk in the cave forms predicts a massive reduction in this neuron. Moreover, the absence of functional eyes in the A. mexicanus Pachón form predicts an even stronger reduction in the cell’s large ventral dendrite that receives visual inputs in sighted fish species. We succeeded in recording in vivo from this neuron in the blind cavefish and two surface tetra (A. mexicanus and Astyanax aeneus), which offers unique chances to simultaneously study evolutionary changes in morphology and function in this giant neuron. In contrast to the predictions, we find that cave life, while sufficient to remove vision, has neither affected the cell's morphology nor its functional properties. This specifically includes the cell's ventral dendrite. Furthermore, cave life did not increase the variance in morphological or functional features. Rather, variability in surface and cave forms was the same, which suggests a complex stabilizing selection in this neuron and a continued role of its ventral dendrite. We found that adult cavefish are potent predators that readily attack smaller fish. So, one of the largely unknown stabilizing factors could be using the MN in such attacks and, in the young fish, escaping them. brain evolution | single neuron evolution | cavefish | neuronal cell type | environmental change

1